Abstract
Key message
Among the 113 lipases present in rice genome, bran and endosperm-specific lipases were identified and lipase activity for one of the selected lipase gene is demonstrated in yeast.
Abstract
Rice bran is nutritionally superior than endosperm as it has major reservoirs of various minerals, vitamins, essential mineral oils and other bioactive compounds, however it is often under-utilized as a food product due to bran instability after milling. Various hydrolytic enzymes, such as lipases, present in bran causes degradation of the lipids present and are responsible for the bran instability. Here, in this study, we have systematically analyzed the 113 lipase genes present in rice genome, and identified 21 seed-specific lipases. By analyzing the expression of these genes in different seed tissues during seed development, we have identified three bran-specific and three endosperm-specific lipases, and one lipase which expresses in both bran and endosperm tissues. Further analysis of these genes during seed maturation and seed germination revealed that their expression increases during seed maturation and decreases during seed germination. Finally, we have shown the lipase activity for one of the selected genes, LOC_Os05g30900, in heterologous system yeast. The bran-specific lipases identified in this study would be very valuable for engineering designer rice varieties having increased bran stability in post-milling.
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Akhter M, Afzal N, Haider Z, Raza MA (2015) Inactivation of lipase enzyme by using chemicals to maximize rice bran shelf life and its edible oil recovery. J Nutr Food Sci S 12:S12002. https://doi.org/10.4172/2155-9600.1000S12002
Akoh CC, Lee GC, Liaw YC, Huang TH, Shaw JF (2004) GDSL family of serine esterases/lipases. Prog Lipid Res 43(6):534–552. https://doi.org/10.1016/j.plipres.2004.09.002
Aravindan R, Anbumathi P, Viruthagiri T (2007) Lipase applications in food industry. Indian J Biotechnol 6(2):141–158
Atapattu N (2013) Effects of citric acid and butylated hydroxytoluene alone or in combination on prevention of rancidity of rice bran during storage. Rice Res Open Access 01:1–5. https://doi.org/10.4172/2375-4338.1000114
Barnes P, Galliard T (1991) Rancidity in cereal products. Lipid Technol 3:23
Barthole G, Lepiniec L, Rogowsky PM, Baud S (2012) Controlling lipid accumulation in cereal grains. Plant Sci 185–186:33–39
Bergonio KB, Lucatin LGG, Corpuz GA, Ramos NC, Duldulao JBA (2016) Improved shelf life of brown rice by heat and microwave treatment. J Microbiol Biotechnol Food Sci 5:378–385. https://doi.org/10.15414/jmbfs.2016.5.4.378-385
Bhardwaj K, Raju A, Rajasekharan R (2001) Identification, purification, and characterization of a thermally stable lipase from rice bran. A new member of the (phospho) lipase family. Plant Physiol 127:1728–1738. https://doi.org/10.1104/pp.010604.1728
Chawla K, Sinha K, Neelam KR, Bhunia RK (2020) Identification and functional characterization of two acyl CoA:diacylglycerol acyltransferase 1 (DGAT1) genes from forage sorghum (Sorghum bicolor) embryo. Phytochemistry 176:112405. https://doi.org/10.1016/j.phytochem.2020.112405
Chen HH, Hung CL, Lin SY, Liou GJ (2015) Effect of low-pressure plasma exposure on the storage characteristics of brown rice. Food Bioprocess Technol 8:471–477. https://doi.org/10.1007/s11947-014-1415-6
de Morais DC, Moraes ÉA, de Dantas MIS, Carraro JCC, da Silva CO, Cecon PR, Martino HSD, Ribeiro SMR (2011) Heat treatment and thirty-day storage period do not affect the stability of omega-3 fatty acid in brown flaxseed (Linum Usitatissimum) whole flour. Food Nutr Sci 2:281–286. https://doi.org/10.4236/FNS.2011.24040
Ding C, Khir R, Pan Z, Zhao L, Tu K, El-Mashad H, McHugh TH (2015) Improvement in shelf life of rough and brown rice using infrared radiation heating. Food Bioprocess Technol 8:1149–1159. https://doi.org/10.1007/s11947-015-1480-5
Doblado-Maldonado AF, Arndt EA, Rose DJ (2013) Effect of salt solutions applied during wheat conditioning on lipase activity and lipid stability of whole wheat flour. Food Chem 140:204–209. https://doi.org/10.1016/j.foodchem.2013.02.071
Dubey BN (2019) Comparative study on the rice bran stabilization processes: a review. Res Dev Mater Sci. https://doi.org/10.31031/rdms.2019.11.000759
Eastmond PJ (2006) Sugar-dependent1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds. Plant Cell 18:665–675. https://doi.org/10.1105/tpc.105.040543
Fraterrigo Garofalo S, Tommasi T, Fino D (2020) A short review of green extraction technologies for rice bran oil. Biomass Convers Biorefinery. https://doi.org/10.1007/s13399-020-00846-3
Gayen D, Ali N, Ganguly M (2014) RNAi mediated silencing of lipoxygenase gene to maintain rice grain quality and viability during storage. Plant Cell Tiss Organ Cult 118:229–243. https://doi.org/10.1007/s11240-014-0476-6
Guevara-Guerrero B, Fernández-Quintero A, Montero-Montero JC (2019) Free fatty acids in rice bran during its storage after a treatment by twin-screw extrusion to prevent possible rapid hydrolytic rancidity of lipids1. DYNA (colombia) 86(208):177–181. https://doi.org/10.15446/dyna.v86n208.72190
Gupta R, Gupta N, Rathi P (2004) Bacterial lipases: an overview of production, purification and biochemical properties. Appl Microbiol Biotechnol 64(6):763–781. https://doi.org/10.1007/s00253-004-1568-8
Guzmán-ortiz FA, Castro-rosas J, Gómez CA, Mora-escobedo R, Rojas-león A, Rodríguez ML, Rodríguez-marín ML (2018) Enzyme activity during germination of different cereals : A review. Food Rev Intl 00(00):1–24. https://doi.org/10.1080/87559129.2018.1514623
Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G (2015) GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics 31:1296–1297. https://doi.org/10.1093/bioinformatics/btu817
Kahlon T (2009) Rice Bran: production, composition, functionality and food applications, physiological benefits. Fiber ingredients. CRC Press, New York. https://doi.org/10.1201/9781420043853-c14
Klein M, Islam Z, Knudsen PB, Carrillo M, Swinnen S, Workman M, Nevoigt E (2016) The expression of glycerol facilitators from various yeast species improves growth on glycerol of Saccharomyces cerevisiae. Metab Eng Commun 3:252–257. https://doi.org/10.1016/j.meteno.2016.09.001
Korneeva OS, Popova TN, Kapranchikov VS, Motina EA (2008) Identification of catalytically active groups of wheat (Triticum aestivum) germ lipase. Appl Biochem Microbiol 44:349–355. https://doi.org/10.1134/S0003683808040029
Lakkakula NR, Lima M, Walker T (2004) Rice bran stabilization and rice bran oil extraction using ohmic heating. Bioresour Technol 92:157–161. https://doi.org/10.1016/j.biortech.2003.08.010
Lavanya MN, Saikiran KCS, Venkatachalapathy N (2019) Stabilization of rice bran milling fractions using microwave heating and its effect on storage. J Food Sci Technol 56:889–895. https://doi.org/10.1007/s13197-018-3550-y
Lescot M, Déhais P, Thijs G et al (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327. https://doi.org/10.1093/nar/30.1.325
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Ma R, Yuan H, An J, Hao X, Li H (2018) A Gossypium hirsutum GDSL lipase/hydrolase gene (GhGLIP) appears to be involved in promoting seed growth in Arabidopsis. PLoS ONE 13:e0195556. https://doi.org/10.1371/journal.pone.0195556
Macedo GA (2010) Seed Lipases: sources, applications and properties—a review. Braz J Chem Eng. https://doi.org/10.1590/S0104-66322010000100002
Mehta A, Bodh U, Gupta R (2017) Fungal lipases: a review. J Biotech Res 8:58–77
Nor N, Muhamad Nordin A, Karim R, Ghazali HM, Adzahan NM, Tauseef Sultan M (2014) Effects of various stabilization techniques on the nutritional quality and antioxidant potential of Brewer’s Rice. J Eng Sci Technol 9(3):347–363
Prakash J (1996) Rice bran proteins: properties and food uses. Crit Rev Food Sci Nutr 36:537–552. https://doi.org/10.1080/10408399609527738
Qian JY, Gu YP, Jiang W, Chen W (2014) Inactivating effect of pulsed electric field on lipase in brown rice. Innov Food Sci Emerg Technol 22:89–94. https://doi.org/10.1016/j.ifset.2014.01.010
Ram H, Gandass N, Sharma A, Singh A, Deshmukh D, Sonah H, Pandey AK, Sharma TR (2020) Spatio-temporal distribution of micronutrients in rice grains and its regulation. Crit Rev Biotechnol 40(4):490–507
Ram H, Singh A, Katoch M, Kaur R, Sardar S, Palia S, Satyam R, Sonah S, Deshmukh R, Pandey A, Gupta I, Sharma TR (2021) Dissecting the nutrient partitioning mechanism in rice grain using spatially resolved gene expression profiling. J Exp Bot 72(6):2212–2230
Rocha-Villarreal V, Serna-Saldivar SO, García-Lara S (2018) Effects of parboiling and other hydrothermal treatments on the physical, functional, and nutritional properties of rice and other cereals. Cereal Chem 95(1):79–91. https://doi.org/10.1002/cche.10010
Schrag JD, Cygler M (1997) Lipases and α/β hydrolase fold. Methods Enzymol 284:85–107. https://doi.org/10.1016/S0076-6879(97)84006-2
Seth S, Chakravorty D, Dubey VK, Patra S (2014) An insight into plant lipase research—challenges encountered. Protein Expr Purif 95:13–21. https://doi.org/10.1016/j.pep.2013.11.006
Sinha K, Kaur R, Singh N, Kaur S, Rishi V, Bhunia RK (2020) Mobilization of storage lipid reserve and expression analysis of lipase and lipoxygenase genes in rice (Oryza sativa var. Pusa Basmati 1) bran during germination. Phytochemistry 180:112538. https://doi.org/10.1016/j.phytochem.2020.112538
Sohail M, Rakha A, Butt MS, Jawad M (2016) Rice bran nutraceutics: a comprehensive review. Crit Rev Food Sci Nutr 57(17):3771–3780. https://doi.org/10.1080/10408398.2016.1164120
Tiwari GJ, Chiang MY, De Silva JR, Song BK, Lau YL, Rahman S (2016) Lipase genes expressed in rice bran: LOC_Os11g43510 encodes a novel rice lipase. J Cereal Sci 71:43–52. https://doi.org/10.1016/j.jcs.2016.07.008
Treichel H, de Oliveira D, Mazutti MA, Di Luccio M, Oliveira JV (2010) A review on microbial lipases production. Food Bioprocess Technol 3(2):182–196. https://doi.org/10.1007/s11947-009-0202-2
Vijayakumar KR, Gowda LR (2013) Rice (Oryza sativa) lipase: molecular cloning, functional expression and substrate specificity. Protein Expr Purif 88:67–79. https://doi.org/10.1016/j.pep.2012.11.011
Xu H, Wei Y, Zhu Y, Lian L, Hongguang X, Cai Q, Chen Q, Lin Z, Wang Z, Huaan X, Zhang J (2015) Antisense suppression of LOX3 gene expression in rice endosperm enhances seed longevity. Plant Biotechnol J 13(4):526–539. https://doi.org/10.1111/pbi.12277
Zhu F (2018) Effect of ozone treatment on the quality of grain products. Food Chem 264:358–366. https://doi.org/10.1016/j.foodchem.2018.05.047
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The funding was funded by DST-INSPIRE Faculty grant from Department of Science and Technology, Govt. of India (Grant no. DST/INSPIRE/04/2016/001118).
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HR conceived and designed the research. SB, SS, KS, MK and RKB performed the experiments. HS and RD contributed to reagents and analytic tools. HR and SB wrote the manuscript. All the authors read and edited the manuscript.
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Communicated by Hiroyasu Ebinuma.
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Fig S1.
Expression patterns of selected 21 lipase genes at Rice Genome Annotation Project database (A) and ePlant database (B). Given expression (FPKM) values are presented as a heatmap (PDF 374 KB)
Fig S2. Expression analysis of selected endosperm specific lipase genes during seed maturation and germination.
Q-PCR analysis of selected three lipases at (A) different seed maturation stages (given as days after fertilization) and (B) seed germination stages (given as days after imbibition). (PDF 50 KB)
Table S1.
Lipase motif containing lipases. (DOCX 27 KB)
Table S2.
Analysis of cis-elements in 1 Kb upstream promoter region of selected bran and endosperm specific genes. (XLSX 32 KB)
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Bansal, S., Sardar, S., Sinha, K. et al. Identification and molecular characterization of rice bran-specific lipases. Plant Cell Rep 40, 1215–1228 (2021). https://doi.org/10.1007/s00299-021-02714-4
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DOI: https://doi.org/10.1007/s00299-021-02714-4